HIGHER CLASSIFICATION OF CALCAREOUS NANNOFOSSILS
Jeremy R. Young, Palaeontology Dept., NHM, Cromwell Road, London, SW7 5BD, UK &Paul R. Bown, Dept. of Geological Sciences, UCL, Gower Street, London, WC1E 6BT, UK

Classification development
The starting point for this overview was the comprehensive review and classification of nannofossils of Perch-Nielsen(1985a, b), complimented by, in particular, the Jurassic nannofossil classification of Bown (1987, 1996) and theclassification of extant haptophytes by Jordan and co-workers (Kleijne, 1993; Green & Jordan, 1994; Jordan & Kleijne,
1994; Jordan & Green, 1994; Jordan et al., 1995). Important earlier sources for these classifications include Parke & Dixon(1976), Hay (1977), Okada & McIntyre (1977) and Tappan (1980). In order to provide a comprehensive synthesis, we paid
special attention to taxonomic papers published since 1985, as catalogued in the INA Bibliography and Index of Taxa. For
the Tertiary, the reviews of Aubry (1984 et seq.) were invaluable sources, although they are based on a slightly different
taxonomic philosophy.

Top-down subdivisions vs bottom-up groupings
Two main approaches can be identified in the classification of calcareous nannofossils. The top-down subdivision approach
has attempted to classify the range of nannofossils into well-defined subdivisions using clear-cut criteria based on major
aspects of shape or structure. For instance, Deflandre (1950) divided all nannofossils into ortholiths and helioliths based onwhether they showed radial calcite orientations (helioliths) or were formed of single calcite crystals (ortholiths, including theconstituent segments of pentaliths). The bottom-up grouping approach, by contrast, has been based on organisation of
species into genera and of genera into families based on multiple similarities of morphology, existence of intergradational
morphologies and stratigraphic distribution. The latter, bottom-up, approach is, we believe, more productive and leads to amore natural classification, and it is the predominant method applied in Perch-Nielsen (1985a, b). This forms the basis for
our formal classification into genera, families and orders. The top-down subdivision approach is, however, valuable fororganising taxa of uncertain inter-relationship and so we apply a system of this type to arrange the higher taxa we recognise
in a logical sequence, and in some cases to provide arbitrary subdivisions of particular taxa.

Incertae sedis and informal categories
A key objective of classification is to systematise our existing knowledge. Conversely, an obvious pitfall of classification isto provide, via spurious pigeon-holing, the impression of knowledge where none exists. To avoid this we have attempted to
discipline ourselves and only to include genera within families (or families within orders) where there is good positive
evidence for doing so. As a consequence, the classification is not comprehensive - many genera are left as of uncertain
family/order, and many families are not assigned to an order. We do not apologise for this, since it is a simple reflection of
the limits of current knowledge.

Use of orders as well as families
The only higher taxonomic category which has been universally applied is family and we continue to use families as themain level of classification. However, in revising the classification, we considered that exclusive use of families was unduly

Nanno classification, JNR 2

restrictive and that, with around 50 families, important relationships would be obscured.
We decided to use orders (Figure 1), rather than to subdivide families, in order to retain as many taxa as possible at theircurrent level, the alternative being to reclassify many well-established families as subfamilies. Also, orders have previously
often been used in nannofossil classifications, notably by Hay (1977), Tappan (1980) and Bown (1987). The principle
potential problem here is discordance with use of orders in the classification of modern haptophytes. Classifications ofmodern haptophytes have, following Parke & Green (in Parke & Dixon, 1976), usually recognised four orders:
Coccosphaerales (coccolith-bearing), Prymnesiales (typical non-coccolith-bearing haptophytes, haptonema well developed),
Isochrysidales (haptonema diminutive, including some coccolith-bearing genera), and Pavlovales (with the flagella ofunequal lengths, the longer flagellum with hairs and scales, haptonema diminutive). Recent work on molecular genetics,
cytology and biochemistry, have unequivocally established the distinctive nature of the Pavlovales and they are now
separated as a discrete class or subclass (Green & Jordan, 1994). The subdivision of the remaining haptophytes into theother three orders has not, however, been supported by subsequent studies, with the result that Green & Jordan (1994)
recommended subsuming all these orders into the single subclass Prymnesiophycidae, order Prymnesiales. Given thisabandonment of the traditional ordinal-level classification of extant haptophytes there is no obvious problem in introducing
a new ordinal-level classification based in the first place on coccolith morphology, although obviously future research on
aspects of haptophyte biology is liable to result at least in modifications of this classification. Nonetheless, this is not an area
where we are especially dogmatic, and debate on use of particular levels of classification would be welcome.

Paraphyletic and polyphyletic taxa
We have not attempted to avoid paraphyletic taxa, i.e. taxa which give rise to other taxa of the same, or higher, level (Figure2). For instance, according to our current understanding of coccolithophore phylogeny, the family Zygodiscaceae isparaphyletic since it is inferred to have given rise to the families Pontosphaeraceae and Helicosphaeraceae. Similarly, thegenus Lophodolithus is paraphyletic if we accept the interpretation that it gave rise to the genus Helicosphaera and family
Helicosphaeraceae. This is manifestly an unavoidable problem in nannofossil systematics since we have abundant evidenceof ancestor-descendant relationships. To give an extreme example, the genera Praeprinsius, Prinsius, Toweius,
Reticulofenestra, Gephyrocapsa, and Emiliania are widely inferred to constitute an evolutionary lineage (e.g. Romein, 1979;
Gallagher, 1989) and so all these, except Emiliania, are paraphyletic.
On the other hand, it is clearly essential to eliminate polyphyletic taxa, i.e. all species included in a higher taxon must have acommon ancestor within that taxon (Figure 2). This is an absolute necessity of a biologically meaningful classification - ifavailable evidence suggests that a taxon contains unrelated sets of species then it must be revised. Of course, we often do notknow for certain whether a group of more or less similar species is directly related or simply a set of convergent
homeomorphs. All taxonomic groupings may be regarded as hypotheses which may be tested through analysis ofmorphology and direct evolutionary data. Our general approach has been to avoid giving taxonomic names to any
subdivisions which we feel are likely to be polyphyletic, for instance we have followed Kleijne (1991) in dividing the large
number of extant holococcolith-bearing genera into two groups based on whether they show dimorphism or not. However,since this character is very likely to have evolved repeatedly, it does not form a suitable basis for grouping the genera into
formal taxa.

Heterococcoliths, holococcoliths and nannoliths

Nanno classification, JNR 3

A special problem with nannofossil taxonomy is the uncertainty as to whether the structures we are examining arehomologous. Indeed, we know that holococcoliths and heterococcoliths are not homologous, whilst we are uncertain as tothe nature of nannoliths. This requires some discussion, and in addition there are separate taxonomic problems associatedwith each of these groupings.

Heterococcoliths
This is the predominant group, usually defined as coccoliths formed of a limited number of complex and variably shaped
crystal-units. The precise scope of the term heterococcolith is vague but there is no dispute that the term is based on typicalextant coccoliths such as those of Coccolithus, Emiliania, Pleurochrysis and Syracosphaera (see also original description ofBraarud et al., 1955). These all share the basic morphology of a rim formed of a radial array of complex crystal-units
surrounding a central-area, with variable structures in the central-area. This basic morphology characterises numerous living
and fossil groups and forms an essential part of most workers' concept of an heterococcolith. There is also evidence that thisis a natural, non-polyphyletic, grouping: (1) studies of evolution in the group tend to indicate a pattern of common origin
and subsequent divergence, with no obvious indications of polyphyly (e.g. Bown, 1987; Romein, 1979; Bown et al., 1992);(2) our ultrastructural research (Young & Bown, 1991; Young et al., 1992; unpublished data) suggests that a widespread,and probably universal, feature of heterococcoliths is V/R mode biomineralisation, i.e. biomineralisation which commenceswith nucleation of a proto-coccolith ring of alternating subvertical and subradial crystal-units, which subsequently develop
to form the rim. This type of biomineralisation is characteristic of all the heterococcolith families recognised here except
possibly the Rhabdosphaeraceae (only V-units definitely identified), Hymenomonadaceae and Papposphaeraceae. V/R modebiomineralisation is a distinctive and sophisticated type of calcification and it seems reasonable to assume that it is a reliable
synapomorphy (shared derived character state), and that the heterococcoliths as a whole form a non-polyphyletic group.

Holococcoliths
Holococcoliths are plainly formed by a very different biomineralisation process to heterococcoliths. Nucleation must occur
across the entire coccolith and the individual crystals retain simple euhedral morphologies. As a result, there is no clear
distinction between the rim and central-area. Moreover, available evidence suggests that calcification occurs extra-cellularly(Rowson et al., 1986), rather than intracellularly. Finally, there are now several well-established cases of holococcoliths andheterococcoliths occurring on alternate phases of the life-cycle of single species. Billard (1994) synthesises this evidence
and suggests that it reflects a haplodiplontic life-cycle, with holococcoliths consistently occurring in the haploid phase. Thisrather suggests that biomineralisation may have evolved independently in the haploid and diploid phases, and that
holococcoliths and heterococcoliths are not meaningfully homologous (Figure 3). Possibly we should consider holococcolithand heterococcolith taxonomy as independent, much as spore and whole-plant taxonomy are.

Holococcolith biomineralisation is distinctive and sophisticated. Crystallite faces are perfectly aligned across large zones,
implying precise control of both a- and c-axis orientation, and the uniformity of crystallite size implies similarly precise
control of nucleation spacing. Like V/R mode biomineralisation in heterococcoliths, it is unlikely that the holococcolithbiomineralisation mode has evolved repeatedly, rather we can regard holococcolith formation as evidence for common
descent of all taxa in which it is developed. Plainly though, both holococcolith formation and heterococcolith formation may
have been lost repeatedly during the evolutionary history of haptophytes. So there is no reason for assuming that all

Nanno classification, JNR 4

holococcoliths will have heterococcolith-bearing phases, or that all species which are known to have both holo- andheterococcolith-bearing phases will be particularly closely related. Future research will certainly help elucidate
relationships. In the interim, it is entirely logical for all holococcolith bearing taxa, without known heterococcolith phases, tobe classified together, in the family Calyptrosphaeraceae.

Unlike heterococcoliths, holococcolith biomineralisation does not provide obvious characters for reliably subdividing thegroup. Homology is difficult to establish since the basic structure appears to consist of a simple mass of crystallites, grossmorphology appears to be of limited value, and there are serious problems due to dimorphism. So at present,
subclassification of the Calyptrosphaeraceae is confined to a rather unsatisfactory, and probably partially artificial, genericclassification. This applies particularly to extant holococcoliths for which crystallographic orientations are poorly known. In
the larger fossil holococcoliths, subdivision into blocks with predictable crystallographic orientations appears to provide a
reasonable basis for classification, but original morphology and possible dimorphism cause separate problems.

Nannoliths
When Braarud et al. (1955) defined the terms heterococcolith and holococcolith, they explicitly described the pentaliths as athird category of similar status. This was a logical proposal since pentaliths show different structures to any heterococcoliths
and it is reasonable to infer they have formed by a significantly different growth/biomineralisation process, and therefore are
not directly homologous. The same applies to numerous other groups, particularly amongst the extinct nannofossils, e.g.
sphenoliths, nannoconids and discoasters. The term nannoliths has been widely used as a collective term for this group (e.g.
Perch-Nielsen, 1985a, b; Bown, 1987; Aubry, 1984 et seq.; Young et al., in press). The most common definition iscalcareous nannofossils of uncertain affinity, but probably related to coccolithophores, i.e. formed by haptophytes.

Although nannoliths are highly variable, several features are repeatedly shown: (1) most nannoliths have morphologies
which are at least suggestive of having been part of a composite exoskeleton; (2) most nannoliths are formed ofmorphologically-complex crystal-units analogous to those of heterococcoliths, although in some cases with evidence ofadditional ultrastructure (e.g. laminae within pentalith crystal-units); (3) for all known nannoliths there are consistent
relationships between morphology and crystallographic orientation; (4) most nannoliths definitely show consistent
handedness or chirality (deviation from radial symmetry), e.g. nannoconids always show clockwise imbrication,
Braarudosphaera sutures are always offset clockwise from the median point of the pentalith edge; (5) nannoliths typicallyhave biogeographic patterns suggesting planktonic origin and as a group are only known from the Triassic to Recent.

These features all suggest close affinities with coccolithophores. Moreover, haptophytes are the only plankton group known
to produce calcareous scales. Dinoflagellates also calcify but they form calcispheres rather than discrete scales. Various
other phytoplankton produce scales, e.g. Prasinophytes and Chrysophytes, but these are either unmineralised or siliceous.
Hence, an assumption that nannoliths are produced by haptophytes has seemed reasonable to phycologists and has been
supported by independent evidence in several cases, e.g. association of ceratoliths and coccoliths (Norris, 1965; Alcober &Jordan, 1997), observation of haptonema on Polycrater (Thomsen et al., 1994), LM observations of typical haptophyte cellfeatures for Braarudosphaera (J. Green, pers. comm., 1996).

Nanno classification, JNR 5

Nannoliths as a whole are, however, almost certainly polyphyletic, probably including: (1) modified heterococcoliths(?Florisphaera, ?polycycloliths, ?helioliths, ?fasciculiths, ?sphenoliths); (2) modified holococcoliths (?ceratoliths,?Lithostromationaceae); (3) and nannoliths formed by entirely different biomineralisation mechanisms (?pentaliths,?Polycrater, ?nannoconids). So they cannot be regarded as a formal taxonomic group, even though it is extremely useful todistinguish them from the more rigorously definable holo- and heterococcoliths. Further research will probably allow someto be reclassified as aberrant heterococcoliths or holococcoliths, whilst others may prove to be discrete groups.

Formal higher classification
The haptophytes were traditionally included in the phylum Chrysophyta along with a range of other golden-brown, scalebearing algae. However, Parke et al. (1955) recognised the haptonema as a unique structure, and following this they wererecognised as a distinct class by Christensen (1962) and division by Hibberd (1972). Rather unfortunately, Hibberd (1976)
argued that the name Haptophyta was unsuitable since it was not based on a generic root. He proposed the alternative name
Prymnesiophyta, and this name was widely used in the literature until recently. However, as noted by Green & Jordan(1994), under the International Code of Botanical Nomenclature, division-level names do not need to be typified and thename Haptophyta has priority. Following from this, the common term haptophyte is preferable to prymnesiophyte; it is also
a less forbidding term so we expect it to rapidly regain universal currency.

Notwithstanding this nomenclatural confusion, the separation of the haptophytes on the grounds of flagellar character has
been well supported by much other evidence from cytology, biochemistry and molecular genetics. There is no dispute thatthey form a discrete algal protist group separable at division/phylum level. Chloroplast colour, however, reflects rather
fundamental aspects of pigment biochemistry, e.g. green algae and land plants all have chlorophyll a and b. By contrast,
golden-brown algae, including haptophytes, have chlorophyll a and c. This unites them with a range of other non-green
algae, including the diatoms and silicoflagellates. Another common feature of this group is that the chloroplasts are
surrounded by four membranes, which is interpreted as the result of a complex endosymbiosis history. Finally, most of thesegroups have two flagella, one short and smooth, the other long and bearing tubular hairs (heterokont). On the basis of this setof shared characters, Cavalier-Smith (1981, 1994) has proposed removing the group from the Protista to form a separate
kingdom, Chromista, also including various protozoa which show the same heterokont flagellation. The haptophytes, as
noted above, have two smooth flagella, and so do not show heterokont flagellation, hence their position in this group issomewhat uncertain, but the general interpretation is that they are a primitive group that diverged prior to the evolution ofheterokont flagellation (e.g. Cavalier-Smith, 1994).

Within the haptophytes, only the single class Prymnesiophyceae is now recognised, divided into two subclasses, thePrymnesiophycidae and Pavlovophycidae (see Green & Jordan, 1994). All coccolithophores belong to the
Prymnesiophycidae, and so to:

Kingdom CHROMISTA Cavalier-Smith, 1981
Division (Phylum) HAPTOPHYTA Hibberd ex Cavalier-Smith, 1986
Class PRYMNESIOPHYCEAE Hibberd, 1976
Subclass PRYMNESIOPHYCIDAE Cavalier-Smith, 1986

Nanno classification, JNR 6

Layout
The same format has been adopted for both of the following papers. For each genus, the original authorship is given,
followed by important synonyms in brackets (). There are then short notes outlining the basis for distinguishing the genus.
Terminology used in these descriptions follows Young et al. (in press). In some places we have included genera which arearguably redundant, and these are placed in square brackets [].

The formal systematic classification is supplemented, as seems useful, by informal groupings. These are numbered andgiven in bold. In most cases, these subdivisions are arbitrary and are likely to prove artificial/polyphyletic, hence they are
not proposed as the bases for future formal classification.

Constraints of space meant it was not practical herein to provide a complete bibliography of taxonomic references. The
references can, however, be found in Perch-Nielsen (1985a, b), and/or the INA Bibliographies.

Nanno classification, JNR 7

References
Alcober, J. & Jordan, R.W. 1997. An interesting association between Neosphaera coccolithomorpha and Ceratolithus
cristatus (Haptophyta). European Journal of Phycology, 32: 91-93.
Aubry, M.-P. 1984 et seq.. Handbook of Cenozoic calcareous nannoplankton. Micropaleontology Press, American Museumof Natural History, New York. Book 1: Ortholithae (Discoasters), 266pp. (1984). Book 2: Ortholithae (Catinasters,
Ceratoliths, Rhabdoliths), 279pp. (1988). Book 3: Ortholithae (Pentaliths, and others), Heliolithae (Fasciculiths,
Sphenoliths and others), 279pp. (1988). Book 4: Heliolithae (Helicoliths, Cribriliths, Lopadoliths and others), 381pp.
(1990).
Billard, C. 1994. Life cycles. In: J.C. Green & B.S.C. Leadbeater (eds). The Haptophyte Algae. Systematics Association
Special Volume, 51, Oxford University Press: 167-186.
Bown, P.R. 1987. Taxonomy, evolution, and biostratigraphy of Late Triassic-Early Jurassic calcareous nannofossils. Special
Papers in Palaeontology, 38: 118.
Bown, P.R. 1996. Recent advances in Jurassic calcareous nannofossil research. Georesearch Forum, 1-2: 55-66.
Bown, P.R. (ed.) In press. Calcareous nannofossil biostratigraphy. British Micropalaeontology Society Series, Chapman &Hall Limited.
Bown, P.R., Burnett, J.A. & Gallagher, L.T. 1992. Calcareous nannoplankton evolution. Memorie di Scienze Geologiche,
43: 1-17.
Braarud, T., Deflandre, G., Halldal, P. & Kamptner, E. 1955. Terminology, nomenclature, and systematics of the
Coccolithophoridae. Micropaleontology, 1: 157-159.
Cavalier-Smith, T. 1981. Eukaryote kingdoms: seven or nine? BioSystems, 10: 93-114.
Cavalier-Smith, T. 1994. Origin and relationships of Haptophyta. In: J.C. Green & B.S.C. Leadbeater (eds). The Haptophyte
Algae. Systematics Association Special Volume, 51, Oxford University Press: 413-436.
Christensen, T. 1962. Alger. In: T.W. Böcher, M. Lange & T. Sorensen (eds). Botanik Bd 2, Systematisk Botanik, Nr. 2,
Munksgaard, Copenhagen: 1-178.
Deflandre, G. 1950. Observations sur les Coccolithophoridés, à propos d'un nouveau type de Braarudosphaeridé,
Micrantholithus, à éléments clastiques. Comptes Rendus de l'Academie des Sciences, 231: 1156-1158.
Gallagher, L.T. 1989. Reticulofenestra: A critical review of taxonomy, structure and evolution. In: J.A. Crux & S.E. van
Heck (eds). Nannofossils and their applications. Ellis Horwood Limited, Chichester: 41-75.
Green, J.C. & Jordan, R.W. 1994. Sytematic history and taxonomy. In: J.C. Green & B.S.C. Leadbeater (eds). The
Haptophyte Algae. Systematics Association Special Volume, 51, Oxford University Press: 1-22.
Hay, W.W. 1977. Calcareous nannofossils. In: A.T.S. Ramsay (ed.). Oceanic Micropaleontology. Academic Press: 10551200.
Hibberd D.J. 1972. Chrysophyta: definition and interpretation. British Phycological Journal, 7: 281.
Hibberd D.J. 1976. The ultrastructure and taxonomy of the Chrysophyceae and Prymnesiophyceae (Haptophyceae): a
survey with some new observations on the ultrastructure of the Chrysophyceae. Botanical Journal of the Linnaen
Society, 72: 55-80.
Jordan, R.W. & Green, J.C. 1994. A check-list of extant haptophyta of the world. Journal of the Marine Biological
Association of the United Kingdom, 74: 149-174.

Nanno classification, JNR 8

Jordan, R.W. & Kleijne, A. 1994. A classification system for living coccolithophores. In: A. Winter & W.G. Siesser (eds).
Coccolithophores. Cambridge University Press: 83-106.
Jordan, R.W., Kleijne, A., Heimdal, B.R. & Green, J.C. 1995. A glossary of the extant haptophyta of the world. Journal of
the Marine Biological Association of the United Kingdom, 75: 769-814.
Kleijne, A. 1991. Holococcolithophorids from the Indian Ocean, Red Sea, Mediterranean Sea and North Atlantic Ocean.
Marine Micropaleontology, 17: 1-76.
Kleijne, A. 1993. Morphology, taxonomy and distribution of extant Coccolithophorids (calcareous nannoplankton). PhD
thesis, FEBO, Enschede, The Netherlands, Vrije University, Amsterdam: 321pp..
Norris, R.E. 1965. Living cells of Ceratolithus cristatus (Coccolithophorinae). Archiv für Protistenkunde, 108: 19-24.
Okada, H. & McIntyre, A. 1977. Modern coccolithophores of the Pacific and North Atlantic Oceans. Micropaleontology, 2:
1-55.
Parke, M. & Dixon, P.S. 1976. Check-list of British marine algae - third revision. Journal of the Marine Biological
Association of the United Kingdom, 56: 579-604.
Parke, M., Manton, I. & Clarke, B. 1955. Studies on marine flagellates. II. Three new species of Chrysochromulina. Journalof the Marine Biological Association of the United Kingdom, 38: 579-609.
Perch-Nielsen, K. 1985a. Mesozoic calcareous nannofossils. In: H.M. Bolli, J.B. Saunders & K. Perch-Nielsen (eds).
Plankton Stratigraphy. Cambridge University Press: 329-426.
Perch-Nielsen, K. 1985b. Cenozoic calcareous nannofossils. In: H.M. Bolli, J.B. Saunders & K. Perch-Nielsen (eds).
Plankton Stratigraphy. Cambridge University Press: 427-554.
Romein, A.J.T. 1979. Lineages in Early Paleogene calcareous nannoplankton. Utrecht Micropalaeontological Bulletins, 22:231pp..
Rowson, J.D., Leadbeater, B.S.C. & Green, J.C. 1986. Calcium carbonate deposition in the motile (Crystallolithus) phase of
Coccolithus pelagicus (Prymnesiophyceae). British Phycological Journal, 21: 359-370.
Tappan, H. 1980. The paleobiology of plant protists. Freeman & Co.: 1028pp..
Thomsen, H.A., Buck, K.R. & Chavez, F.P. 1994. Haptophytes as components of marine phytoplankton. In: J.C. Green &B.S.C. Leadbeater (eds). The Haptophyte Algae. Systematics Association Special Volume, 51, Oxford University Press:
187-208.
Young, J.R., Bergen, J.A., Bown, P.R., Burnett, J.A., Fiorentino, A., Jordan, R.W., Kleijne, A., van Niel, B.E., Romein,
A.J.T. & von Salis, K. In press. Guidelines for coccolith and calcareous nannofossil terminology. Palaeontology, 40.
Young, J.R. & Bown, P.R. 1991. An ontogenetic sequence of coccoliths from the Late Jurassic Kimmeridge Clay of
England. Palaeontology, 34: 843-850.
Young, J.R., Didymus, J.M., Bown, P.R., Prins, B. & Mann, S. 1992. Crystal assembly and phylogenetic evolution inheterococcoliths. Nature, 356: 516-518.

Nanno classification, JNR 9

Figure 1: Proposed heterococcolith orders. Sketches illustrate distal views, and side-views with interpreted cut-away crosssections. Vertical thickness of cycles is sometimes exaggerated to clarify structure.

Nanno classification, JNR 10

Figure 2: Holophyletic, paraphyletic and polyphyletic taxa.

Nanno classification, JNR 11

Figure 3: Diagram showing how current observations on haptophyte life-cycles can be resolved into a consistent phylogeny.

Nanno classification, JNR 12